Human Striatal Response to Salient Nonrewarding Stimuli

Abstract

Although one proposed function of both the striatum and its major dopamine inputs is related to coding rewards and reward-related stimuli, an alternative view suggests a more general role of the striatum in processing salient events, regardless of their reward value. Here we define saliency as an event that both is unexpected and elicits an attentional-behavioral switch (i.e., arousing). In the present study, human striatal responses to nonrewarding salient stimuli were investigated. Using functional magnetic resonance imaging (fMRI), the blood oxygenation level-dependent signal was measured in response to flickering visual distractors presented in the background of an ongoing task. Distractor salience was manipulated by altering the frequency of distractor occurrence. Infrequently presented distractors were considered more salient than frequently presented distractors. We also investigated whether behavioral relevance of the distractors was a necessary component of saliency for eliciting striatal responses. In the first experiment (19 subjects), the distractors were made behaviorally relevant by defining a subset of them as targets requiring a button press. In the second experiment (17 subjects), the distractors were not behaviorally relevant (i.e., they did not require any response). The fMRI results revealed increased activation in the nucleus accumbens after infrequent (high salience) relative to frequent (low salience) presentation of distractors in both experiments. Caudate activity increased only when the distractors were behaviorally relevant. These results demonstrate a role of the striatum in coding nonrewarding salient events. In addition, a functional subdivision of the striatum according to the behavioral relevance of the stimuli is suggested.

The Formation of Abnormal Associations in Schizophrenia: Neural and Behavioral Evidence

“…The ventral striatum plays a central role in reward processing and it has been suggested that activations of the ventral striatum normally mediate the incentive or motivational salience of environmental stimuli (Jensen et al, 2003(Jensen et al, , 2007Zink et al, 2003Zink et al, , 2004Zink et al, , 2006. The stronger responses to the neutral stimulus among patients may reflect an aberrant attribution of motivational salience to neutral stimuli (Kapur, 2003).…”

Low dopamine striatal D2 receptors are associated with prefrontal metabolism in obese subjects: Possible contributing factors

“…There is also evidence that DA modulates the somatosensory cortex in the human brain (Kuo et al, 2007). Inasmuch as DA stimulation signals saliency and facilitates conditioning (Zink et al, 2003, Kelley, 2004), DA's modulation of the somatosensory cortex's response to food is likely to play a role in the formation of conditioned association between food and food-related environmental cues and in the enhanced reinforcing value of food that occurs in obesity (Epstein et al, 2007).…”

Young adult stimulant users' increased striatal activation during uncertainty is related to impulsivity

“…Salient stimuli are those that, by virtue of their intensity or importance, increase attention, arousal, and mobilization of behavioral resources, thus contributing to action (Horvitz, 2000;Redgrave et al, 1999). Recent neuroimaging work has demonstrated in humans that the striatum, a key reinforcement-related dopaminergic target structure (Robbins and Everitt, 1996), is also responsive to reward and nonreward salience (Zink et al, 2003;Zink et al, 2004). Aron et al (2004), meanwhile, have found that individuals' response uncertainty in a nonreward category learning task predicts midbrain activation, which, in turn, predicts ventral striatal and medial frontal response to negative feedback.…”